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TECHNICAL REPORTS

Plant and Environment Interactions

Competitive Mobilization of Phosphate and Arsenate Associated with Goethite by Root Activity

^a UFZ Helmholtz Centre for Environmental Research, Dep. of Soil Ecology, Theodor-Lieser-Str. 4, 06120 Halle, Germany
^b Soil Science and Soil Protection Group, Inst. of Agriculture and Nutritional Sciences, Martin Luther Univ. Halle-Wittenberg, Weidenplan 14, 06108 Halle/Saale, Germany
^c UFZ Helmholtz Centre for Environmental Research, Dep. of Analytical Chemistry, Permoserstr. 15, 04318 Leipzig, Germany
^d UFZ Helmholtz Centre for Environmental Research, Department of Soil Chemistry, Theodor-Lieser-Str. 4, 06120 Halle, Germany

^* Corresponding author (doris.vetterlein{at}ufz.de).

Received for publication September 14, 2006.

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION Materials and Methods Results Discussion Conclusions REFERENCES

 
Arsenate (As^V) is the predominant form of arsenic in soils under aerobic conditions and competes with the major plant nutrient phosphorus (P) in the form of phosphate (P^V) not only for sorption sites on mineral surfaces in soil but also for root membrane transporters. Plants have evolved several mechanisms for the mobilization of P^V in soils in response to P deficiency, such as the release of organic anions and protons. The aim of the present study was to test whether these mechanisms result in a simultaneous mobilization of arsenate and what would be the consequences for As transfer from soil to plant. The compartment system approach with Zea mays as model crop was chosen as an experimental setup. The system is equipped with micro suction cups and allowed us to investigate processes occurring in the vicinity of roots. As a case study, an artificial quartz substrate with well defined soil physical properties was fertilized, spiked with As^V, and amended with increasing amounts of goethite (0, 1, and 4 g kg^–1 in treatments G-0, G-1, and G-4, respectively). The addition of goethite alleviated the As^V-induced growth reduction and reduced As^V transfer from the substrate to the plant but induced P deficiency at the same time. When low amounts of goethite (1 g kg^–1) were added, plants mobilized P^V but not As^V, which might be related to differences in surface complexation reported for P^V and As^V. No mobilization of P^V or As^V was observed with the addition of higher amounts of goethite, probably because of decreasing competition between organic anions, P^V, and As^V for binding sites.

Abbreviations: As^III, arsenite • As^V, arsenate • DAP, days after planting • P^V, phosphate

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION Materials and Methods Results Discussion Conclusions REFERENCES

 
ARSENIC (As) is toxic to humans and other living organisms and presents potentially serious environmental problems. Arsenic in the environment is often associated with other elements (Au, Ag, Cu, Fe, S, and Sn in particular), and mining and processing of respective ores has led to extensive pollution of mining regions throughout the world (Morin and Calas, 2006; Nriagu, 1994).

Processing of ores in the catchment area is the origin of arsenic contamination in the alluvial soils along the river Mulde in Germany, which show As concentrations in the range of 30 to 437 mg kg^–1. A survey of the federal state of Saxony (Klose, personal communication) revealed that about 80% of these soils are polluted with total As concentrations well above the threshold value for pasture of 50 mg kg^–1 (BBodSchV: German legislation providing background and threshold levels for concentration in soils which distinguish between different forms of land use. For grassland, which might be used as fodder for animals, the threshold level for As in aqua regia extract is 50 mg kg^–1.) Thus, there is increasing concern about As transfer into the food chain. Abatement strategies require to understand controlling factors and processes. Arsenate (As^V) is the predominant As form in soils under aerobic conditions, whereas arsenite (As^III) occurs predominantly in reduced environments (Masscheleyn et al., 1991; Smith et al., 1998). The mobility of As in soils depends on several factors, including redox potential, soil mineralogy, pH, and the presence of other ligands, in particular oxyanions, that compete with As for soil retention sites. The main process controlling the mobility of As in the soil-water-plant systems is the adsorption of As by soil constituents rather than precipitation of As minerals (Goldberg and Glaubig, 1988; Livesey and Huang, 1981; Roy et al., 1986). Goethite is the most widespread Fe-oxide in soils and mineral weathering environments. In soils of cool and temperate zone, goethite is commonly the sole pedogenic Fe-oxide (Schwertmann and Taylor, 1989).

Laboratory experiments (Gao and Mucci, 2001; Hingston et al., 1971; Manning and Goldberg, 1996) and field studies (Fordham and Norrish, 1974) have demonstrated that the variable charge mineral goethite is a strong sorbent for As^V and phosphate (P^V) (Geelhoed et al., 1997; Hingston et al., 1971; Manning and Goldberg, 1996). The sorption of As^V on the surface of goethite decreases with increasing soil solution pH as the number of negative charges on the surface of the sorbent increases, and it decreases with increasing P^V concentrations in the soil solution, which can be expressed as increasing molar P^V:As^V ratio (Gao and Mucci, 2001; Hingston et al., 1971; Manning and Goldberg, 1996; Violante and Pigna, 2002).

Some authors found a higher affinity of the goethite surface for As^V than for P^V (Gao and Mucci, 2001; Violante and Pigna, 2002), whereas others reported similar affinities for P^V and As^V (Hiemstra and Van Riemsijk, 1999; Manning and Goldberg, 1996, 1997). The differences may be related to differences in the ionic strength of the solution or to the nature of surface complexation.

Phosphate is considered an analog of As^V, having similar chemical properties and behaviors. They are both oxyanions in aqueous solutions with three similar acid dissociation constants.

Phosphorus, in contrast to arsenic, is a major plant nutrient. As a response to P deficiency, many plant species exude organic anions from their roots, which mobilizes P and enhances uptake of P. Well known examples of such plant species are crucifers (e.g., rape and mustard), legumes (e.g., lupin and chickpea) (Dinkelaker et al., 1989; Gerke and Meyer, 1995; Hoffland et al., 1989; Li et al., 1997), and a range of other species (e.g., maize). For maize roots, enhanced efflux of citrate and malate has been observed in response to nutrient stress at rates of 1.4 and 6.0 nmol mg^–1 root h^–1 in sterile systems (Jones and Darrah, 1995).

Plants can alter the pH in the vicinity of the roots as a response to P deficiency (Hinsinger et al., 2003). Such pH changes in the rhizosphere are a result of unbalanced cation and anion uptake and a corresponding proton release to maintain electro-neutrality. Respective pH changes are reported to be in the range of 1 to 1.5 pH units (Nye, 1981; Gerke et al., 1994).

Phosphate and As^V can be mobilized from goethite surface by organic anions or pH changes (Geelhoed et al., 1998, 1999; Grafe et al., 2001; Liu et al., 2001). However, the efficiency of organic anions in releasing As^V or P^V from goethite may differ substantially (e.g., oxalate ions in solution desorbed higher amounts of P^V than As^V) (Liu et al., 2001).

Phosphate and As^V do not only compete for sorption sites on mineral surfaces but also for root membrane transporters. It is well documented that As^V is taken up via the high-affinity P transporters (Meharg and Macnair, 1992; Meharg and Hartley-Whitaker, 2002). These transporters show a higher affinity for P^V than for As^V (Meharg and Hartley-Whitaker, 2002), and the molar P^V:As^V ratio in soil or nutrient solution has a strong effect on the uptake of As^V. Esteban et al. (2003) have shown that increasing the molar P^V:As^V ratio in nutrient solution from 1 to 4 reduced As^V uptake by 70%. Phosphorus-deficient plants take up more As^V from nutrient solution at same molar P^V:As^V ratio because those plants increase the number of high-affinity P transporters (Meharg and Hartley-Whitaker, 2002).

Although increasing P^V concentration in nutrient solution is an efficient way to decrease As^V uptake in solution cultures, this is not necessarily true for soil-cultivated plants, as P fertilizer trials have shown (Heeraman et al., 2001). In soils, applied fertilizer P can compete with As^V for binding sites and thus increase As^V concentrations in soil solution.

Arsenate competes with P^V for binding sites on the goethite surface and at the P transporters in the root membranes. This competition is potentially affected by organic anion and proton release occurring under P deficiency. Thus, the aim of the present experiment was to study the interactions of P^V, As^V, and goethite in soil–plant transfer under controlled conditions in a system that allowed us to investigate related processes occurring in the vicinity of the roots.

The experiment was designed (i) to study the effect of increasing amounts of goethite on P^V and As^V concentrations in soil solution and the resulting molar P^V:As^V ratio; (ii) to monitor soil solution concentrations of As^V, P^V, Fe, and H⁺ in the bulk soil, rhizosphere, and root compartment with time to detect whether plants are able to mobilize P^V or As^V from goethite under P deficiency; (iii) to measure temporal changes of the molar P^V:As^V ratio in the root compartment and its effect on As^V uptake and distribution in the plant; and (iv) to follow As speciation in the rhizosphere soil solution.

The level of P^V was chosen to achieve adequate P supply in the control treatment (G-0) throughout the growing period. Arsenate supply was selected to induce growth depression in the G-0 treatment without visual deleterious effects. An artificial quartz substrate was used not only to obtain well defined soil physical properties but as a system in which the number and kind of surface sorption sites can be easily manipulated by the addition of well defined mineral phases like goethite, which was applied in increasing amounts. As a consequence of the low sorption capacity of the artificial substrate solution, concentrations of As^V and P^V are high in this case study compared with conditions found in the real world.

The compartment system approach was chosen as experimental setup, using Zea mays as a model crop. A detailed discussion of this approach, based on the formation of a root mat, can be found in Vetterlein and Jahn (2004). A description of this approach by a rhizosphere model with chemical speciation, based on the geochemical code PHREEQC coupled with MATLAB for transport calculation, is given in Szegedi et al. (2007). Plants and microbes growing in the system were the only sources of organic matter.

	Materials and Methods

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Experimental Design
Zea mays L. cv. Rivaldo (two plants per compartment system) was grown under controlled conditions (25°C day/23°C night; 40/60% relative humidity; 12 h photoperiod with 350 µmol m² s^–1) in boxes in which the root compartment (88 x 32 x 100 mm) was separated from the bulk soil compartments (88 x 105 x 100 mm) by a nylon net (30 µm, hydrophilic) (Fig. 1 in Vetterlein and Jahn, 2004). The root mat formed along the nylon net is regarded as the root surface. Thus, the system enables measurements of rhizosphere processes with sensors installed at known distances from the nylon net (root surface). The soil extending from the nylon net into the bulk soil compartment is designated as rhizosphere. Microtensiometers (ø 1.3 mm) (Vetterlein et al., 1993) and micro suction cups (ø 1.3 mm, ceramic made from Kawenit) (Göttlein et al., 1996) were aligned horizontally with spatial resolution of 30 and 6 mm, respectively.

View larger version (10K): [in this window] [in a new window]   Fig. 1. Change of initial arsenate (AsV) and phosphate (PV) concentration and their molar ratio in soil solution with increasing amounts of goethite application to the artificial quartz substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1). Soil solution was sampled after allowing 6 d for equilibration. Values given represent the mean of all suction cup positions within each treatment.

No As was detected in the initial substrate mixture. The substrate was initially supplied with 100 mg N kg^–1 (NH₄NO₃), 80 mg P kg^–1 (CaHPO₄), 100 mg K kg^–1 (K₂SO₄), 100 mg Ca kg^–1 (CaSO₄ x 2H₂O), 50 mg Mg kg^–1 (MgCl₂), a micronutrient solution (3.25 mg Mn kg^–1 [MnSO₄ x 2H₂O]), 0.79 mg Zn kg^–1 (Zn[NO₃]₂ x 4H₂O), 0.5 mg Cu kg^–1 (CuSO₄ x 5 H₂O and 0.17 mg B kg^–1 [H₃BO₃]), and 3.25 mg Fe kg^–1 (Fe-EDTA). The substrate was spiked with 5 mg As^V kg^–1 (Na₂HAsO₄ x 7H₂O), a level sufficient to induce growth depression in Zea mays without occurrence of visual symptoms. After adding N, K, Mg, and micronutrients as solutions, the substrate was allowed to dry before it was thoroughly mixed and sieved. Thereafter, P and Ca were mixed in as powder, and As^V was mixed in as solution. The substrate was again air dried.

Three treatments (G-0, G-1, and G-4) were established by the addition of 0, 1, and 4 g goethite (-FeOOH) kg^–1. The goethite was mixed into the air-dried substrate the day before the substrate (moistened to 1% [w/w]) was packed into the compartment systems. The packed compartment systems were placed on a sand bed of 5 cm height and moistened by capillary rise by addition of deionized water to the sand bed. At this time, all the sensors were installed. The first collection of soil solution took place 6 d later, which corresponds to 3 days after planting (DAP) pre-germinated corn seeds into the root compartment.

To avoid undesired As contamination by the addition of goethite, the goethite used was synthesized using a modified version of the procedure described by Atkinson et al. (1967). Ferric nitrate (0.2 M) solution was slowly titrated with KOH in a plastic bottle until the pH reached 12. The resulting ferrihydrite suspension was aged for 72 h at 55°C. The goethite, which had settled to the bottom of the container, was dialyzed against deionized water until the electrical conductivity was <50 µS dm^–1. The freeze-dried goethite, sieved <63 µm, was characterized by X-ray diffraction (DIFFRAC plus-D5005; Software EVA), and surface area (BET N₂ adsorption) measurements were conducted on a NOVA 4000 (Quantachrome Instruments) surface area analyzer; the surface area was 129 m² g^–1. The synthesized goethite contained an oxalate-extractable fraction of 10% (Fe_o/Fe_d ratio 0.1). Because X-ray diffraction analysis did not show any sign of ferrihydrite-like phases (data not shown), this oxalate-extractable fraction might be from the dissolution of very small goethite crystals (Weidler et al., 1998).

Compartment systems were moistened to soil matric potential of –3 kPa (measured at 40 mm height), which corresponds to 22% (v/v) soil moisture according to the soil moisture release curve established for the substrate with a bulk density of 1.45 g cm³.

Soil Solution Sampling and Analysis
Soil solution was sampled simultaneously from all micro suction cups 3, 10, 17, 24, and 31 DAP. Solution was collected for 2 h at a suction of 30 kPa on respective days. Soil moisture, monitored by microtensiometers with a temporal resolution of 10 min, was maintained within the range of 18.5 to 22% (v/v) throughout the duration of the experiment by applying deionized water to the sand bed. The results for the first sampling date (3 DAP) are presented as mean values over all 15 suction cup positions in each treatment because plant-induced changes were not present at that stage of the experiment.

Immediately after collecting soil solutions, bulk samples were made from the three replications of each treatment for each suction cup position. Samples were stored at 8°C, and measurement of arsenic species by IC-ICP-MS (Mattusch et al., 2000) was conducted within 24 h after sampling. Fe²⁺ and total Fe concentrations were determined colorimetrically according to the US-Standard Method 3500-Fe D and DIN 38406 E1 (EPOS Analyzer 5060; Eppendorf AG, Germany); P (detection limit 0.2 mg L^–1), K, Ca, Mg, S, Mn, and total As concentrations were determined by ICP–OES (Jobin Yvon); and NH₄⁺ and NO₃^– concentrations were determined by flow stream analyzer (Skalar). Soil solution pH in the small volumes (100–600 µL) was determined with an ISFET electrode (IQ240-06 with PH16 SS).

The initial soil solution composition and surface sorption in the different treatments were calculated using PHREEQC taking quartz, gypsum, FePO₄, CaHPO₄, CO₂, and goethite for treatment G-1 and G-4 as equilibrium phases and taking into account the presence of EDTA. With increasing goethite addition, the fraction of P^V adsorbed to goethite increased (from 0 to 7 and 30% in G-0, G-1, and G-4, respectively), and the fraction of P^V in soil solution decreased (Table 1 ). The calculated surface coverage of the goethite (maximum adsorption capacity 2.85 µmol m^–2) was 82 and 54% for P^V in G-1 and G-4, respectively, and 4 and 8% for As^V in G-1 and G-4 using different equilibrium constants for weak and strong binding sites. Details are described by Szegedi et al. (2007).

View this table: [in this window] [in a new window]   Table 1. Partitioning of phosphate (PV) between different solid species and soil solution with increasing amounts of goethite application to the artificial substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1) at the beginning of the experiment.

Differences between treatments were tested by one-factorial ANOVA (SPSS, Version 14.0) at P < 0.05. Standard deviations are given in all graphs except for those based on measurements in bulk samples (As^V, P^V, pH, Fe, and As^III).

	Results

TOP NOTES ABSTRACT INTRODUCTION Materials and Methods Results Discussion Conclusions REFERENCES

 
In the artificial quartz substrate with the given fertilizer additions, a level of As contamination of 5 mg kg^–1 in the form of As^V was chosen because preliminary trials revealed that this level resulted in a growth depression of about 30% for roots and shoots of Zea mays compared with a control treatment without As contamination.

Phosphate concentrations were always higher than As^V concentrations. The addition of goethite decreased As^V concentrations in the soil solutions more than P^V concentrations (Fig. 1). Accordingly, molar P^V:As^V ratios in the soil solutions increased with increasing addition of goethite at the start of the experiment (Fig. 1).

Neither depletion nor accumulation of As^V in the rhizosphere (extending from the nylon net into the bulk soil) was observed during the 32-d experiment (Fig. 2 ). Initial differences in As^V concentrations between the different goethite treatments remained throughout the duration of the experiment.

View larger version (27K): [in this window] [in a new window]   Fig. 2. Effect of increasing amounts of goethite application to the artificial quartz substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1) on soil solution arsenate (AsV) concentration at increasing distance from the center of the root compartment with time. Horizontal hair lines at 16 mm distance from the center of the root compartment represent the location of the nylon net (root surface). Soil solution was sampled 10, 17, 24, and 31 d after planting (DAP).

View larger version (27K): [in this window] [in a new window]   Fig. 3. Effect of increasing amounts of goethite application to the artificial quartz substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1) on soil solution phosphate (PV) concentration at increasing distance from the center of the root compartment with time. Horizontal hair lines at 16 mm distance from the center of the root compartment represent the location of the nylon net (root surface). Soil solution was sampled 10, 17, 24, and 31 d after planting (DAP). *No sample was available.

View larger version (15K): [in this window] [in a new window]   Fig. 4. Temporal pattern of molar phosphate (PV):arsenate (AsV) ratio in the soil solution of the root compartment with increasing amounts of goethite application to the artificial substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1). In treatment G-4, the ratio could only be calculated for 3 and 10 d after planting; thereafter, PV concentrations were close to zero. The bars, representing SD, refer to the variation between the five suction cups positioned in the root compartment.

View larger version (15K): [in this window] [in a new window]   Fig. 5. Effect of increasing amounts of goethite application to the artificial substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1) on the concentration of arsenic (As) in different organs of Zea mays 32 d after planting. A different scale had to be selected for concentrations in the roots. Means for the different treatments were separated by Tukey test. For each plant organ, means followed by the same letter were not significantly different from each other.

View larger version (17K): [in this window] [in a new window]   Fig. 6. Effect of increasing amounts of goethite application to the artificial substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1) on shoot and root dry matter of Zea mays 32 d after planting. Means for the different treatments were separated by Tukey test. For each plant organ, means followed by the same letter were not significantly different from each other.

View larger version (33K): [in this window] [in a new window]   Fig. 7. Effect of increasing amounts of goethite application to the artificial quartz substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1) on soil solution pH at increasing distance from the center of the root compartment with time. Horizontal hair lines at 16 mm distance from the center of the root compartment represent the location of the nylon net (root surface). Soil solution was sampled 10, 17, 24, and 31 d after planting (DAP).

View larger version (26K): [in this window] [in a new window]   Fig. 8. Effect of increasing amounts of goethite application to the artificial quartz substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1) on soil solution iron (Fe) concentration at increasing distance from the center of the root compartment with time. Horizontal hair lines at 16 mm distance from the center of the root compartment represent the location of the nylon net (root surface). Soil solution was sampled 10, 17, 24, and 31 d after planting (DAP).

	Discussion

TOP NOTES ABSTRACT INTRODUCTION Materials and Methods Results Discussion Conclusions REFERENCES

 
The decrease of As^V and P^V concentrations in soil solution with increasing addition of goethite to the system is in line with results from batch experiments showing the ability of goethite to adsorb As^V and P^V (Gao and Mucci, 2001; Geelhoed et al., 1997; Manning and Goldberg, 1996). The increase in molar P^V:As^V ratio with increasing goethite addition indicates a higher affinity of goethite for As^V than for P^V. Such a higher affinity for As^V than for P^V was also reported by Gao and Mucci (2001) and Violante and Pigna (2002) and might be related to differences in the nature of surface complexation for As^V and P^V. Arsenate forms predominantly inner-sphere bidentate complexes (Fendorf et al., 1997; Sun and Doner, 1996; Waychunas et al., 1993), whereas inner-sphere monodentate complexes might dominate for P^V (Tejedor-Tejedor and Anderson, 1990; Persson et al., 1996).

The initial As^V and P^V concentrations in soil solution in the present experiment ranged from 0.01 mM (G-4) to 0.15 mM (G-0) for As^V and from 0.17 to 0.80 for P^V. This wide concentration range and the relatively high values for P^V and As^V, which are in the same order of magnitude as found at a contaminated reference site along the river Mulde (0.005–0.063 mM As^V and 0.05–0.14 mM P^V), were a result of several restrictions associated with the compartment system and the artificial substrate.

The amount of nutrient required is defined by the tissue concentration for adequate growth and the biomass expected for the growing period. Apart from this, the size of the system (soil volume) determines the final nutrient concentration in soil. Soil solution concentration (mM) is then a function of this soil concentration (mg kg^–1), the soil water content, and the solid and gaseous equilibrium phases. Thus, despite the high soil solution P concentrations at the start of the experiment, as a result of goethite application and increasing nutrient requirement during the time course of the experiment, plants became P deficient in treatments G-1 and G-4. Phosphorus concentrations decreased below the detection limit of ICP–OES in the root compartment 31 DAP in treatment G-4.

The nutritional status of a plant cannot be predicted from soil (solution) concentration alone. To derive fertilizer recommendations, such relationships are empirically derived for field-grown plants, where roots can explore a very large soil volume (Marschner, 1995). They do not hold for plants growing in a limited soil volume for a certain time period. For the nutrient status of a plant, the important factor is whether the nutrient requirement during a certain time interval (nutrient concentration x plant biomass) can be met by the nutrient uptake during this time interval. For a given root with a certain uptake capacity, soil solution nutrient concentration in its vicinity is constant if the amount of nutrient transported to the root surface matches plant uptake capacity for this nutrient per unit time and if no mobilization or immobilization of the nutrient in question is induced by changes in rhizosphere chemistry. Accumulation of the nutrient occurs if the amount transported to the root surface exceeds the uptake capacity or if the mobility of the nutrient increases (Hinsinger, 2001; Marschner, 1995). Such an increase due to altered mobility has been described by Kirk (2002) and by Geelhoed et al. (1999) as a result of citrate release in P-deficient plants. Depletion is found if uptake capacity exceeds the amount of nutrient transported to the surface or if sorption or precipitation occurs, as has been reported by Dinkelaker et al. (1989) for calcium citrate. Depletion is a prerequisite for diffusion (transport along a chemical gradient) toward the root surface coming into play as a relevant transport process. As growth rate (and hence water uptake), root-shoot ratio (and hence uptake per unit root length), P requirement for growth, exudation of protons, and organic acid release all change with time in a different manner, nutrient gradients in the rhizosphere, which result from the interplay of all these parameters with soil chemistry and soil transport processes (mass flow, diffusion), must be highly dynamic. This is illustrated by Kirk (2002), who neglected mass flow, and by Geelhoed et al. (1999), who considered mass flow in their model calculations in which they predicted soil solution P concentration profiles with increasing distance from the root surface. In both models, the release of citrate by roots in response to P deficiency is considered, and citrate degradation with time and interaction with P adsorbed on surfaces or P in mineral phases is taken into account as well as citrate diffusion away from the root surface. Both models predict, for certain time intervals, a strong increase of soil solution P concentration close to the root surface and a decrease within the first millimeter from the root surface. With time, in the case of Kirk's model from 7 to 35 d, the steepness of gradients decreases. These predictions are in close agreement with the soil solution P concentration gradients observed in the present experiment in treatment G-1 (Fig. 3), except that we did not find a decrease within the first millimeter from the root surface (nylon net). However, given the limited spatial resolution of the suction cup sampling method, this is not surprising.

Plants in treatment G-4 showed even lower P concentrations in the leaves compared with G-1 and were thus also P deficient. The question arises why no P^V mobilization was observed in this treatment.

In G-1 and G-4 treatments, a strong decrease of pH was observed in the root compartment and in the rhizosphere. As the number of negative charges on the surface of the goethite increases with increasing pH the sorption of P^V, As^V and organic anions (citrate) on the goethite surface decreases with increasing pH and increases with decreasing pH (Gao and Mucci, 2001; Grafe et al., 2001; Hingston et al., 1971; Manning and Goldberg, 1996). According to model calculations of Geelhoed et al. (1999) using the CD-MUSIC approach, citrate causes the largest desorption of P^V from goethite at pH 4.5 to 5.

For CaHPO₄, which is, apart from the P fraction adsorbed to goethite, the major P fraction in the system (Table 1), the solubility increases with decreasing pH in pure systems (Brown and Chow, 1976). However, in extrapolating to our experimental system, the presence of additional anions and cations and the increasing ionic strength has to be taken into account. Although a similar range of pH values was measured in G-1 and G-4, the increase of P concentration with decreasing pH value is much more pronounced in G-1 compared with G-4 (Fig. 10), indicating that an additional factor is influencing P solubility in G-1, which might be present in G-4 but is not effective. This additional factor is likely the presence of organic anions.

View larger version (14K): [in this window] [in a new window]   Fig. 10. Effect of increasing amounts of goethite application to the artificial quartz substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1) on the relationship between soil solution pH and phosphate (PV) concentration over all sampling times and suction cup positions.

Differences in the nature of surface complexation and thus the affinity of P^V and As^V for goethite explains why roots were able to increase P^V concentrations in the soil solution from the root compartment and from the rhizosphere in treatment G-1, whereas the As^V concentration remained unchanged. Organic anions, to be released when plants are P deficient (Geelhoed et al., 1999; Jones and Darrah, 1995), like in treatments G-1 and G-4, have a larger effect on the desorption of P^V than on the desorption of As^V from the goethite surface (Liu et al., 2001). This is further supported by findings of Geelhoed et al. (1998) and Grafe et al. (2001); their findings revealed that equimolar citrate concentrations reduced P^V adsorption to goethite but had no effect on As^V sorption to the surface of goethite regardless of whether As^V or citrate was added first.

Decreases in pH not only alter the charges on the surface of the goethite but can also result in the dissolution of Fe-oxides. Oxalate-extraction, which is conducted at pH 3.0, has shown that about 10% of the goethite synthesized for our experiments was extractable, which is an indication for the presence of very small goethite crystals. Very small goethite crystals, in contrast to larger ones, have a higher specific surface area and are more easily dissolved at low pH in the presence of organic anions (Strauss et al., 1997; Weidler et al., 1998). Such a partial dissolution of the Fe-oxide added to the substrate is in line with the observation that Fe concentrations in soil solution from the root compartment and from the rhizosphere increased with time in treatment G-1 and G-4 (Fig. 8). However, dissolution of a small fraction of the Fe-oxide added (about 1% of the amount added in G-1) had no effect on the concentrations of As^V and P^V in soil solution.

Increases in Fe concentration in the soil solution from the root compartment and rhizosphere in treatments G-1 and G-4 might also be related to the release of phytosiderophores because maize is a strategy II plant (Marschner and Römheld, 1994; Reichard et al., 2005). Even though Fe analyses showed similar Fe concentrations in all treatments (75 mg kg^–1 in young leaves) and visual signs of Fe deficiency did not occur, this possibility cannot be ruled out because Fe-sufficient plants release some phytosiderophores. Alternatively, increases in Fe concentration in the soil solution might be related to Fe complexation with organic anions released by the roots. Such a mechanism was suggested by Fitz et al. (2003), who observed an increase of Fe concentration in rhizosphere soil solution to correspond to an increase in dissolved organic carbon concentration in a study with the As hyperaccumulator Pteris vittata.

A reductive dissolution of Fe-oxides (Jones et al., 2000; Roden and Zachara, 1996) cannot be ruled out as a cause for the increased Fe concentrations in the vicinity of roots. Lower redox potentials in the vicinity of roots compared with the bulk soil have been reported by Flessa and Fischer (1992) and Fiedler et al. (2004) as a result of root respiration and root exudates as substrate for microbial activity. Because the root mat represents a very high concentration of roots per unit surface area, microsites with lower redox potential might be created, although half of the pore volume was filled with air at a water content of 22% (v/v). Decreasing redox potentials in the vicinity of roots would be in line with the observation of increasing concentrations of As^III in the soil solution from the root compartment and from the rhizosphere in some treatments (Fig. 9 ). However, As^III is observed in treatment G-0 and G-1 and not in G-4, although root mass was similar in G-1 and G-4 (Fig. 6). To clarify this point, soil redox potential measurement should be conducted in further experiments. The analysis of As species in the plant material stored in liquid nitrogen may help to identify the source of As^III in soil solution.

View larger version (25K): [in this window] [in a new window]   Fig. 9. Effect of increasing amounts of goethite application to the artificial quartz substrate (G-0 = 0 g kg–1; G-1 = 1 g kg–1; G-4 = 4 g kg–1) on soil solution arsenite (AsIII) concentration at increasing distance from the center of the root compartment with time. Horizontal hair lines at 16 mm distance from the center of the root compartment represent the location of the nylon net (root surface). Soil solution was sampled 10, 17, 24, and 31 d after planting (DAP).

	Conclusions

TOP NOTES ABSTRACT INTRODUCTION Materials and Methods Results Discussion Conclusions REFERENCES

 
Goethite is a strong sorbent for As^V but also for P^V; thus, the addition of goethite may reduce the risk of As^V transfer in soil–plant systems, but there is a chance of inducing P deficiency by this measure. Under certain conditions (treatment G-1), plants were able to mobilize P^V but not As^V, which might be related to the difference in surface complexation reported for P^V and As^V. To further elucidate the effect of root exudates on the mobilization of P^V and As^V, analysis of organic anions in soil solution samples is necessary. Mobilization of As^V from the goethite surface in the vicinity of roots might also occur as a result of reductive dissolution of Fe-oxides due to a decrease of soil redox potential. Therefore, the present compartment system should be equipped with a system for measuring redox potential with high spatial resolution in future studies. The As^III found in soil solution in the root compartment is not necessarily formed in the soil but might be released from the roots. Arsenic species analysis of plant material should be conducted to elucidate this point. Because goethite is not the only Fe-oxide in alluvial soils, similar studies should be conducted for other minerals, such as ferrihydrite, that are known to adsorb As^V and P^V but differ in surface area and crystallinity.

	ACKNOWLEDGMENTS

 
This work was conducted in the framework of the BASS Helmholtz-Univ. Young Investigators Group, supported by the Helmholtz Association Germany. We thank the reviewers and the editor for their valuable comments and Robert Mikutta for conducting the X-ray diffraction analysis of the goethite.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION Materials and Methods Results Discussion Conclusions REFERENCES

 
All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.

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